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Intracortical connections are not required for oscillatory activity in the visual cortex

Published online by Cambridge University Press:  02 June 2009

Geoffrey M. Ghose
Affiliation:
Group in Vision Science, School of Optometry, University of California, Berkeley, CA 94720, USA
Ralph D. Freeman
Affiliation:
Group in Vision Science, School of Optometry, University of California, Berkeley, CA 94720, USA

Abstract

Synchronized oscillatory discharge in the visual cortex has been proposed to underlie the linking of retinotopically disparate features into perceptually coherent objects. These proposals have largely relied on the premise that the oscillations arise from intracortical circuitry. However, strong oscillations within both the retina and the lateral geniculate nucleus (LGN) have been reported recently. To evaluate the possibility that cortical oscillations arise from peripheral pathways, we have developed two plausible models of single cell oscillatory discharge that specifically exclude intracortical networks. In the first model, cortical oscillatory discharge near 50 Hz in frequency arises from the integration of signals from strongly oscillatory cells within the LGN. The model also predicts the incidence of 50-Hz oscillatory cells within the cortex. Oscillatory discharge around 30 Hz is explained in a second model by the presence of intrinsically oscillatory cells within cortical layer 5. Both models generate spike trains whose power spectra and mean firing rates are in close agreement with experimental observations of simple and complex cells. Considered together, the two models can largely account for the nature and incidence of oscillatory discharge in the cat's visual cortex. The validity of these models is consistent with the possibility that oscillations are generated independently of intracortical interactions. Because these models rely on intrinsic stimulus-independent oscillators within the retina and cortex, the results further suggest that oscillatory activity within the cortex is not necessarily associated with the processing of high-order visual information.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1997

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References

Abeles, M. (1991). Corticonics: Neural Circuits of the Cerebral Cortex. Cambridge, Massachusetts: Cambridge University Press.Google Scholar
Ahissar, E. & Vaadia, E. (1990). Oscillatory activity of single units in a somatosensory cortex of an awake monkey and their possible role in texture analysis. Proceedings of the National Academy of Sciences of the U.SA. 87, 89358939.CrossRefGoogle Scholar
Arnett, D. (1975). Correlation analysis in the cat dLGN. Experimental Brain Research 24, 111130.Google Scholar
Beaulieu, C. & Colonnier, M. (1985). A laminar analysis of the number of round-asymmetric and flat-symmetric synapses on spices, dendritic trunks, and cell bodies in area 17 of the cat. Journal of Comparative Neurology 231, 180189.Google Scholar
Bernander, Ö., Douglas, R.J., Martin, K.A.C. & Koch, C. (1991). Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proceedings of the National Academy of Sciences of the U.S.A. 88, 1156911573.CrossRefGoogle ScholarPubMed
Bishop, P.O., Levick, W.R. & Williams, W.O. (1964). Statistical analysis of the dark discharge of lateral geniculate neurons. Journal of Physiology 170, 598612.Google Scholar
Bishop, P.O., Coombs, J.S. & Henry, G.H. (1973). Receptive fields of simple cells in the cat striate cortex. Journal of Physiology 231, 3160.Google Scholar
Bonds, A.B. (1989). Role of inhibition in the specification of orientation selectivity of cells in the cat striate cortex. Visual Neuroscience 2, 4155.CrossRefGoogle ScholarPubMed
Bullier, J. & Henry, G.H. (1979). Ordinal position of neurons in cat striate cortex. Journal of Neurophysiology 42, 12511281.CrossRefGoogle ScholarPubMed
Burke, R.E. (1967). Composite nature of the monosynaptic excitatory postsynaptic potential. Journal of Neurophysiology 30, 11151137.CrossRefGoogle ScholarPubMed
Bush, P.C. & Douglas, R.J. (1991). Synchronization of bursting action potential discharge in a model network of neocortical neurons. Neural Computation 3, 1930.CrossRefGoogle Scholar
Chagnac-Amatai, Y. & Connors, B.W. (1989). Synchronized excitation and inhibition driven by intrinsically bursting neurons in neocortex. Journal of Neurophysiology 62, 11491162.CrossRefGoogle Scholar
Chapman, B., Zahs, K.R. & Stryker, M.P. (1991). Relation of cortical cell orientation selectivity to alignment of receptive fields of the ge-niculocortical afferents that arborize within a single orientation column in ferret visual cortex. Journal of Neuroscience 11, 13471358.CrossRefGoogle ScholarPubMed
Cleland, B.G., Dubin, M.W. & Levick, W.R. (1971). Simultaneous recording of input and output of lateral geniculate neurones. Nature: New Biology 231, 191192.Google Scholar
Colonnier, M. (1981). The electron-microscopic analysis of the neuronal organization of the cerebral cortex. In Organization of the Cerebral Cortex, ed. Adelman, G., Dennis, S.G., Schmitt, F.O. & Worden, F.G., pp. 125153. Cambridge, Massachusetts: MIT Press.Google Scholar
Cragg, B.G. (1975). The development of synapses in the visual system of the cat. Journal of Comparative Neurology 160, 147166.CrossRefGoogle ScholarPubMed
Crick, F. & Koch, C. (1990). Some reflections on visual awareness. Cold Spring Harbor Symposiums on Quantitative Biology 55, 953962.Google Scholar
DeAngelis, G.C., Robson, J.R., Ohzawa, I. & Freeman, R.D. (1992). Organization of suppression in receptive fields of neurons in cat visual cortex. Journal of Neurophysiology 68, 144163.CrossRefGoogle ScholarPubMed
Dinse, H.R., Krüger, K., Mallot, H.A. & Best, J. (1991). Temporal structure of cortical information processing: Cortical architecture, oscillations, and non-separability of spatio-temporal receptive field organization. In Neuronal Cooperativity, ed. Krüger, J., pp. 68104. Berlin: Springer-Verlag.Google Scholar
Douglas, R.J., Martin, K.A.C. & Whitteridge, D. (1988). Selective responses of visual cortical cells do not depend on shunting inhibition. Nature 332, 642644.Google Scholar
Douglas, R.J., Martin, K.A.C. & Whitteridge, D. (1991). An intracellular analysis of the visual responses of neurones in cat visual cortex. Journal of Physiology 440, 659696.CrossRefGoogle ScholarPubMed
Douglas, R.J., Koch, C., Mahowald, M., Martin, K.A.C., & Suarez, H.H. (1995). Recurrent excitation in neocortical circuits. Science 269, 891985.Google Scholar
Eckhorn, R., Bauer, R., Jordan, W., Brosch, M., Kruse, W., Munk, M. & Reitboeck, H.J. (1988). Coherent oscillations: A mechanisms of feature linking in the visual cortex? Biological Cybernetics 60, 121130.CrossRefGoogle ScholarPubMed
Eeckman, F. & Freeman, W. (1990). Correlations between unit firing and EEG in the rat olfactory system. Brain Research 528, 238244.CrossRefGoogle ScholarPubMed
Engel, A.K., König, P., Gray, C.M. & Singer, W. (1990). Stimulus-dependent neuronal oscillations in cat visual cortex: Inter-columnar interaction as determined by cross-correlation analysis. European Journal of Neuroscience 2, 588606.CrossRefGoogle ScholarPubMed
Engel, A.K., König, P., Kreiter, A.K. & Singer, W. (1991 a). Interhemispheric synchronization oscillatory neuronal responses in cat visual cortex. Science 252, 11771179.Google Scholar
Engel, A.K., Kreiter, A.K., König, P. & Singer, W. (1991 b). Synchronization of oscillatory neuronal responses between striate and extra-striate visual cortical areas of the cat. Proceedings of the National Academy of Sciences of the U.S.A. 88, 60486052.CrossRefGoogle Scholar
Engel, A.K., König, P., Kreiter, A.K., Gray, C.M. & Singer, W. (1991 c). Temporal coding by coherent oscillations as a potential solution to the binding problem: Physiological evidence. In Nonlinear Dynamics and Neural Networks, ed. Schuster, H.G., pp. 149163. New York: VCH Weinheim.Google Scholar
Engel, A.K., König, P., Kreiter, A.K., Schillen, T.B. & Singer, W. (1992). Temporal coding in the visual cortex: New vistas on integration in the nervous system. Trends in Neuroscience 15, 218226.CrossRefGoogle ScholarPubMed
Ferster, D. & Lindström, S. (1983). An intracellular analysis of geniculocortical connectivity in area 17 of the cat. Journal of Physiology 342, 181215.CrossRefGoogle ScholarPubMed
Ferster, D. (1987). Origin of orientation-selective EPSPs in simple cells of cat visual cortex. Journal of Neuroscience 7, 17801791.Google Scholar
Ferster, D. & Jagadeesh, B. (1992). EPSP-IPSP interactions in cat visual cortex studied with in vivo whole-cell patch recording. Journal of Neuroscience 12, 12621274.Google Scholar
Ferster, D., Chung, S. & Wheat, H.S. (1996). Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 380, 249252.CrossRefGoogle ScholarPubMed
Fetz, E.E. & Gustafsson, B. (1983). Relation between shapes of postsynaptic potentials and changes in firing probability of cat motoneurones. Journal of Physiology 341, 387410.CrossRefGoogle ScholarPubMed
Garey, L.F. & Powell, T.P.S. (1971). An experimental study of the termination of the lateral genicocortical pathway in the cat and monkey. Proceedings of the Royal Society B 179, 4163.Google Scholar
Gerstner, W., Ritz, R. & Van Hemmen, J.L. (1993). A biologically motivated and analytically soluble model of collective oscillations in the cortex. Biological Cybernetics 68, 363374.Google Scholar
Ghose, G.M. & Freeman, R.D. (1992). Oscillatory discharge in the visual system: Does it have a functional role? Journal of Neurophysiology 68, 15581574.Google Scholar
Ghose, G.M., Freeman, R.D. & Ohzawa, I. (1994). Local intracortical connections in the cat's visual cortex: Postnatal development and plasticity. Journal of Neurophysiology 72, 12901303.CrossRefGoogle ScholarPubMed
Granit, C., Kernell, D. & Lammarre, Y. (1966). Algebraic summation in the synaptic activation of motorneurons firing within the primary range to injected currents. Journal of Physiology (London) 187, 379399.CrossRefGoogle Scholar
Gray, C.M. & Singer, W. (1989). Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proceedings of the National Academy of Sciences of the U.S.A. 86, 16981702.Google Scholar
Gray, C.M., Engel, A.K., König, P. & Singer, W. (1990). Stimulus-dependent neuronal oscillations in cat visual cortex: Receptive-field properties and feature dependence. European Journal of Neuroscience 2, 607619.CrossRefGoogle ScholarPubMed
Gray, C.M., Engel, A.K., König, P. & Singer, W. (1992). Synchronization of oscillatory neuronal responses in cat striate cortex: Temporal properties. Visual Neuroscience 8, 337347.Google Scholar
Guido, W., Lu, S.-M., Sherman, S.M. (1992). Relative contributions of burst and tonic responses to the receptive field properties of lateral geniculate neurons in the cat. Journal of Neurophysiology 68, 21992211.Google Scholar
Hamos, J.E., Van Horn, S.C., Raczkowski, D. & Sherman, S.M. (1987). Synaptic circuits involving an individual retinogeniculate axon in the cat. Journal of Comparative Neurology 259, 165192.Google Scholar
Heeger, D.J. (1993). Modeling simple-cell direction selectivity with normalized, half-squared, linear operators. Journal of Neurophysiology 70, 18851898.Google Scholar
Hirsch, J.A. & Gilbert, C.D. (1991). Synaptic physiology of horizontal connections in the cat's visual cortex. Journal of Neuroscience 11, 18001809.CrossRefGoogle ScholarPubMed
Holt, G.R., Softky, W.R., Koch, C. & Douglas, R.J. (1996). Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. Journal of Neurophysiology 75, 18061814.Google Scholar
Hornung, J.P. & Garey, L.J. (1981). The thalamic projection to cat visual cortex: Ultrastructure of neurons identified by Golgi impregnation or retrograde horseradish peroxidase transport. Journal of Neuroscience 6, 10531068.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology (London) 160, 106154.CrossRefGoogle ScholarPubMed
Ito, H., Gray, C.M. & Viana Di Prisco, P. (1994). Can oscillatory activity in the LGN account for the occurrence of synchronous oscillations in the visual cortex? Society of Neuroscience Abstracts 20, 134.Google Scholar
Jagadeesh, B., Ferster, D. & Gray, C. (1992). Visually evoked oscillations of membrane potential in cells of cat visual cortex. Science 257, 552554.CrossRefGoogle ScholarPubMed
Jagadeesh, B., Wheat, H.S. & Ferster, D. (1993). Linearity of summation of synaptic potentials underlying direction selectivity in simple cells of the cat visual cortex. Science 262, 19011904.Google Scholar
Kato, N., Kawaguchi, S., Yamamoto, T., Samejima, A. & Miyata, H. (1983). Postnatal development of the geniculocortical projection in the cat: Electrophysiological and morphological studies. Experimental Brain Research 51, 6572.CrossRefGoogle ScholarPubMed
Kiper, D.C., Gegenfurtner, K.R. & Movshon, J.A. (1996). Cortical oscillatory responses do not affect visual segmentation. Vision Research 36, 539544.CrossRefGoogle Scholar
Koch, C., Poggio, T. & Torre, V. (1983). Nonlinear interactions in a dendritic tree: Localization, timing, and role in information processing. Proceedings of the National Academy of Sciences of the U.S.A. 80, 27992802.Google Scholar
Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 188, 285307.Google Scholar
Langdon, R.B. & Sur, M. (1990). Components of field potentials evoked by white matter stimulation in isolated slices of primary visual cortex: Spatial distributions and synaptic order. Journal of Neurophysiology 64, 14841501.Google Scholar
Lankheet, M.J.M., Molenaar, J. & van de Grind, W.A. (1989). The spike generating mechanism of cat retinal ganglion cells. Vision Research 29, 505517.Google Scholar
Laufer, M. & Verzeano, M. (1967). Periodic activity in the visual system of the cat. Vision Research 7, 215229.CrossRefGoogle ScholarPubMed
Lehky, S.R. & Maunsell, J.H.R. (1996). No binocular rivalry in the LGN of alert macaque monkeys. Vision Research 36, 12251234.Google Scholar
LeVay, S. & Gilbert, C.D. (1976). Laminar patterns of geniculocortical projection in the cat. Brain Research 113, 119.CrossRefGoogle ScholarPubMed
LeVay, S. (1986). Synaptic organization of claustral and geniculate affer-ents to the visual cortex of the cat. Journal of Neuroscience 6, 35643575.CrossRefGoogle Scholar
Levine, M.W. & Troy, J.B. (1985). The variability of the maintained discharge of cat dorsal lateral geniculate cells. Journal of Physiology (London) 375, 339359.Google Scholar
Llinás, R.R., Grace, A.A. & Yarom, Y. (1991). In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range. Proceedings of the National Academy of Sciences of the U.S.A. 88, 897901.CrossRefGoogle ScholarPubMed
Lu, S.-M., Guido, W. & Sherman, S.M. (1992). Effects of membrane voltage on receptive field properties of lateral geniculate neurons in the cat: Contributions of the low-threshold Ca2+ conductance. Journal of Neurophysiology 68, 12851298.CrossRefGoogle ScholarPubMed
Malpeli, J.G. (1983). Activity of cells in area 17 of the cat in absence of input from layer A of later geniculate nucleus. Journal of Neurophysiology 49, 595610.CrossRefGoogle Scholar
Martin, K.A.C. (1984). Neuronal circuits in cat striate cortex. In Cerebral Cortex, Volume 2, ed. Peters, A. & Jones, E.G., pp. 241284. New York: Plenum Press.CrossRefGoogle Scholar
Martin, K.A.C. (1988). The Wellcome Prize Lecture: From single cells to simple circuits in the cerebral cortex. Quarterly Journal of Experimental Physiology 73, 637702.Google Scholar
McCormick, D.A., Gray, C. & Wang, Z. (1993). Chattering cells: A new physiological subtype which may contribute to 20–60 Hz oscillations in cat visual cortex. Society for Neuroscience Abstracts 19, 869.Google Scholar
McGuire, B.A., Gilbert, C.D., Rivlin, P.K. & Wiesel, T.N. (1991). Targets of horizontal connections in macaque primary visual cortex. Journal of Comparative Neurology 305, 370392.Google Scholar
Melssen, W.J. & Epping, W.J.M. (1987). Detection and estimation of neural connectivity based on crosscorrelation analysis. Biological Cybernetics 57, 403414.CrossRefGoogle ScholarPubMed
Mitzdorf, U. & Singer, W. (1978). Prominent excitatory pathways in the cat visual cortex (A 17 and A 18): A current source density analysis of electrically evoked potentials. Experimental Brain Research 33, 371394.Google Scholar
Morrone, M.C., Burr, D.C. & Maffei, L. (1982). Functional implications of cross-orientation inhibition of cortical visual cells. Proceedings of the Royal Society B (London) 216, 335354.Google ScholarPubMed
Movshon, J.A. (1993). Symposium: Cortical oscillatory responses and feature binding. Society for Neuroscience Abstracts 19, 1054.Google Scholar
Mukherjee, P. & Kaplan, E. (1995). Dynamics of neurons in the cat lateral geniculate nucleus: In vivo electrophysiology and computational modeling. Journal of Neurophysiology 74, 12221243.CrossRefGoogle ScholarPubMed
Munemori, J., Hara, K., Kimura, M. & Sato, R. (1984). Statistical features of impulse trains in cat's lateral geniculate neurons. Biological Cybernetics 50, 167172.Google Scholar
Neuenschwander, S. & Singer, W. (1996). Long-range synchronization of oscillatory light responses in the cat retina and lateral geniculate nucleus. Nature 379, 728733.CrossRefGoogle ScholarPubMed
Noest, A.J. & Koenderink, J.J. (1991). Do coherent oscillations help or hinder feature linking? (Abstract). Investigative Ophthalmology and Vision Science (Suppl.) 32, 907.Google Scholar
Perkel, D.H. (1965). Applications of a digital computer simulation of a neural network. In Biophysics and Cybernetic Systems, ed. Maxfield, M., Callahan, A. & Fogel, L.J., pp. 2641. Washington D.C.: Spartan Books.Google Scholar
Perkel, D.H., Gerstein, G.L. & Moore, G.P. (1967). Neuronal spike trains and stochastic point processes. II. Stimulataneous spike trains. Biophysics Journal 7, 419440.CrossRefGoogle Scholar
Peters, A. & Payne, B.R. (1993). Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. Cerebral Cortex 3, 6978.CrossRefGoogle ScholarPubMed
Peters, A., Payne, B.R. & Budd, J. (1994). A numerical analysis of the geniculocortical input to striate cortex in the monkey. Cerebral Cortex 4, 215229.CrossRefGoogle ScholarPubMed
Pinault, D. & Deschenes, M. (1992). Voltage-dependent 40-Hz oscillations in rat reticular thalamic neurons in vivo. Neuroscience 51, 245258.CrossRefGoogle ScholarPubMed
Reinis, S., Weiss, D.S. & Landolt, J.P. (1988). Mass correlograms of multiple neuronal activity in the cat's extrastriate cortex. Biological Cybernetics 59, 103107.CrossRefGoogle ScholarPubMed
Robson, J.G. & Troy, J.B. (1987). Nature of the maintained discharge of Q, X, and Y retinal ganglion cells of the cat. Journal of the Optical Society of America A 4, 23012307.CrossRefGoogle Scholar
Salin, P.A., Bullier, J. & Kennedy, H. (1989). Convergence and divergence in the afferent projections to cat area 17. Journal of Comparative Neurology 283, 486512.CrossRefGoogle ScholarPubMed
Schwark, H.D., Malpeli, J.G., Weyand, T.G. & Lee, C. (1986). Cat area 17. II. Response properties of infragranular layer neurons in the absence of supragranular layer activity. Journal of Neurophysiology 56, 10741087.CrossRefGoogle ScholarPubMed
Schwarz, C. & Bolz, J. (1991). Functional specificity of a long-range horizontal connection in cat visual cortex: A cross-correlation study. Journal of Neuroscience 11, 29953007.Google Scholar
Segundo, J.P., Perkel, D.H., Wyman, H., Hegstad, H. & Moore, G.P. (1968). Input-output relations in computer-simulated nerve cells. Ky-bernetik 4, 157171.Google ScholarPubMed
Sillito, A.M. (1975). The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. Journal of Physiology (London) 250, 305329.CrossRefGoogle Scholar
Sillito, A.M., Jones, H.E., Gerstein, G.L., & West, D.C. (1994). Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex. Nature 369, 479482.Google Scholar
Silva, L.R., Amitai, Y. & Connors, B.W. (1991). Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. Science 251, 432435.CrossRefGoogle ScholarPubMed
Singer, W., Tretter, F. & Cynader, M. (1975). Organization of cat striate cortex: A correlation of receptive field properties with afferent and efferent connections. Journal of Neurophysiology 38, 10801098.Google Scholar
Singer, W. (1990). Search for coherence: A basic principle of cortical self-organization. Concepts of Neuroscience 1, 126.Google Scholar
Somers, D.C., Nelson, S.B., & Sur, M. (1995). An emergent model of orientation selectivity in cat visual cortical simple cells. Journal of Neuroscience 15, 54485465.Google Scholar
Sompolinsky, H., Golomb, D. & Kleinfeld, D. (1990). Global processing of visual stimuli in a neural network of coupled oscillators. Proceedings of the National Academy of Sciences of the U.S.A. 87, 72007204.CrossRefGoogle Scholar
Steriade, M. & Llinás, R.R. (1988). The functional states of the thalamus and the associated neuronal interplay. Physiology Review 68, 649742.Google Scholar
Tanaka, K. (1983). Cross-correlation analysis of geniculostriate neuronal relationships in cats. Journal of Neurophysiology 49, 13031318.CrossRefGoogle ScholarPubMed
Toyama, K., Kimura, M. & Tanaka, K. (1981). Organization of cat visual cortex as investigated by cross-correlation technique. Journal of Neurophysiology 45, 202214.Google Scholar
Traub, R.D., Miles, R. & Wong, R.K.S. (1989). Model of the origin of rhythmic population oscillations in the hippocampal slice. Science 243, 13191325.CrossRefGoogle ScholarPubMed
Traub, R.D., Whittington, M.A., Stanford, I.M. & Jefferys, J.G.R. (1996). A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature 383, 621624.Google Scholar
Troy, J.B. & Robson, J.G. (1992). Steady discharges of X and Y retinal ganglion cells of cat under photopic illuminance. Visual Neuroscience 9, 535553.CrossRefGoogle ScholarPubMed
Ts'o, D.Y., Gilbert, C.D. & Wiesel, T.N. (1986). Relationships between horizontal interactions and functional architecture in cat striate cortex as reveal by cross-correlation analysis. Journal of Neuroscience 6, 11601170.CrossRefGoogle ScholarPubMed
von der Malsburg, C. & Buhmann, J. (1992). Sensory segmentation with coupled neural oscillators. Biological Cybernetics 67, 233242.CrossRefGoogle ScholarPubMed
Wilson, M.A. & Bower, J.M. (1991). A computer simulation of oscillatory behavior in primary visual cortex. Neural Computation 3, 498509.CrossRefGoogle ScholarPubMed
Young, M.P., Tanaka, K., & Yamane, S. (1992). On oscillating neuronal responses in the visual cortex of the monkey. Journal of Neurophysiology 67, 14641474.Google Scholar